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Salt Gland Function in the Green Sea Turtle Chelonia Mydas

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Salt Gland Function in the Green Sea Turtle Chelonia Mydas / exp. Biol. 144, 171-184 (1989) 171 Wrinted in Great Britain © The Company of Biologists Limited 1989 SALT GLAND FUNCTION IN THE GREEN SEA TURTLE CHELONIA MYDAS BY SARAH W. NICOLSON AND PETER L. LUTZ Division of Biology and Living Resources, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, USA Accepted 2 February 1989 Summary When salt-gland-cannulated green sea turtles were stimulated by the intra- venous injection of various salt loads the secretion osmolality rose quickly from a basal value of 300-400 mosmol kg"1 to a plateau of 1680-2000. The height of the plateau and the duration of the response were dependent on the amount of salt given. An increase in flow rate accompanied the initial rise in concentration, but the flow rate thereafter declined while the plateau concentration was held. The fluid was protein-free, and was mainly composed of Na+ and CP, in similar relative concentrations to those in sea water, but had substantial amounts of K+, Mg2"1" and HCC>3~ and negligible amounts of glucose. Urea concentrations did not change with osmolarity, and were similar to that of plasma, suggesting that the walls of the salt gland ducts are permeable to urea. The composition of the tears was uninfluenced by the concentration of the injected solutions, and its ionic content did not directly depend upon the identity of the added salts. The two eyes of individual turtles frequently did not function in synchrony. The average amount of the salt load remaining in a turtle at the end of salt gland activity, 4-5mmolionkgbodymass~1, was very similar to the median load required to stimulate the salt gland (4-0mmolion kg body mass"1). This suggests that there is a threshold salt load level of around 4-5 mmol ion kg body mass"1 that determines salt gland on/off activity. The flow/concentration relationships of the salt gland fluid are consistent with water reabsorption from a primary isosmotic secretion being the major mechanism for concentrating the tears. A high maximal secretory rate is indicated for the primary fluid, 0-32 ml g salt gland-1min~1, equivalent to that of the mammalian kidney. Calculations suggest that 83 % of the initial fluid is recovered, Na+ is passively concentrated, Cl~ and Mg2"1" concentrations are enhanced, and that the duct walls are either impermeable to glucose or that glucose is actively taken up. Introduction Marine vertebrates exist in a medium that is three times the concentration of their internal fluids, and so face the problems of water loss and ion gain. With the apparent exception of the marine mammals, the kidneys of these animals are words: osmoregulation, salt excretion, water balance, ion regulation. 172 S. W. NlCOLSON AND P. L. LUTZ insufficient to handle the salt influx and, therefore, all marine vertebrates have extrarenal mechanisms for excreting salt. In elasmobranchs, birds and reptiles, discrete salt glands are present (Holmes & Phillips, 1985; Burger & Hess, 1960). In marine turtles, the salt glands have been shown to be the major route for sodium and potassium excretion (Holmes & McBean, 1964; Evans, 1973; Kooistra & Evans, 1976). The organs used as salt glands in different organisms are nonhomologous and have apparently evolved independently (Peaker & Linzell, 1975). Ion secretion occurs in the rectal glands of sharks (Burger & Hess, 1960), the sublingual glands of snakes (Dunson et al. 1971), the nasal glands of birds and lizards, and the post- orbital glands of turtles (Peaker & Linzell, 1975). Despite their nonhomologous origins, the salt glands of these different organisms are all characterized micro- scopically by principal cells with large quantities of mitochondria and convoluted lateral, and sometimes basal, membranes (Ellis & Abel, 1964; Peaker & Linzell, 1975). The similarity in the structure of the salt glands of different species suggests that there may be similarities in salt gland operation as well. There is evidence of hypertrophy in response to long-term increases in salt loading in both birds and turtles (Peaker & Linzell, 1975; Cowan, 1969, 1971). The diet of marine turtles consists of a variety of marine invertebrates or, in the case of the green turtle (Chelonia my das), various marine grasses and algae. Since marine invertebrates and plants are generally similar in salt content, and contain three times as much salt kg body water"1 as sea turtles (Holmes & McBean, 1964), the salt burden for feeding turtles could be considerable. The importance of the gland for hatchling turtles was suggested by the work of Bennett et al. (1986), who found that hatchling loggerhead turtles {Caretta caretta) dehydrated rapidly in sea water unless allowed to drink. Since cloacal loss of ions was found to be negligible, the salt glands were assumed to be responsible for maintaining osmotic balance. Salt glands appear to play an integral part in the adaptation of turtles to the marine environment, yet surprisingly little is known about the functioning of these organs. Primary data on lachrymal fluid composition, on the rate and pattern of flow, or on salt gland response to stimulation are either limited or non-existent, especially in comparison to birds or sharks. The purpose of this study was to describe the parameters of a typical salt gland response, to determine how a sea turtle controls salt gland output and to examine the importance of the glands in the salt economy of the sea turtle. The parameters examined included tear content and concentration, the duration of the salt gland response, the flow rate of fluid (tears) from the gland during the response and the percentage of a given salt load excreted. Materials and methods Eight juvenile green turtles ranging in mass from 6 to 19 kg were kept outdoors in large 1-2m x 2m fibreglass tanks with a flow-through, sand-filtered seawater system. Turtles were fed Purina Turtle Chow daily or every other day. Salt gland function in the turtle 173 Animals were not fed for at least 24 h prior to an experiment, and were not used again for at least 14 days following experiments involving cannulation, or 7 days following experiments not involving cannulation. Animals were allowed to acclimate to the laboratory for at least 1 h before an experiment was begun. Cannulation of the salt gland was accomplished using the technique of D. Hudson (personal communication). PE-90 tubing was positioned under the posterior corner of the turtle's eyelid and gently moved into the duct of the salt gland. The tubing was taped to the head of the turtle to prevent slippage. Throughout the secretory period, samples of salt gland fluid were collected into polyethylene microcentrifuge tubes attached to the cannula. When secretions were too viscous to move through the tube of their own accord, collection was aided by the application of suction up to 70 kPa using a peristaltic pump or a hand- held vacuum pump. Because the cannulae were unable to collect all of the secretions, total salt gland output was measured by placing a funnel under the chin and capturing all the secreted fluid in graduated tubes positioned under the funnel. Flow was measured by recording how much fluid was collected during each 15 min sampling period. In some cases the sampling periods were 30 or 60 min if the flow was low. The duration of the salt gland response was measured from the sampling period in which tear concentration was observed to begin rising until it fell to below SOOmosmolkg"1. The sample-collecting containers attached to each cannula were replaced every 15 min if flow was sufficient or every 30 or 60 min. Samples were measured immediately for osmolality using a Wescor vapour pressure osmometer (model 5100B) and were sealed and stored frozen until other analyses could be performed. Only tears collected by the cannulae were used for analyses to avoid the possibility of contamination by other fluids. Sodium and potassium were measured by flame photometry (Coleman model 21), chloride by an Aminco chloride titrator and for magnesium a Perkin-Elmer 403 atomic absorption spectrophotometer was used. Urea was measured using Sigma urea-nitrogen kit no. 66-UV and glucose by the use of Sigma glucose kit no. 115. Protein was measured using the Bradford (Biorad) and Lowry (Lowry etal. 1951) assay methods. To measure bicarbonate and pH, a radiometer blood microsystem (BMS3 Mk 2) was used. Fresh, anaerobically collected tear samples were injected directly from the cannula into the sample chamber and pH and the partial pressure of carbon dioxide (PcoJ were measured with electrodes. Bicarbonate concentration was calculated using the Henderson-Hasselbalch equation: pH = pK' + ([HCO3~]/ aPcoJ- The solubility coefficient of carbon dioxide was estimated by extrapolating the change in a with chlorinity at 20°C (values obtained from Riley & Skirrow, 1965) to the approximate concentration of the tears. Likewise, pK', the first apparent dissociation constant of carbonic acid, was approximated by interpolat- ing between known values for pK' at chlorinities higher and lower than tears at 20°C (values obtained from Riley & Skirrow, 1965). Appropriate standards were fcun with all measurements. 174 S. W. NlCOLSON AND P. L. LUTZ 2000- I 00 f 1500' o .1 1000- 500- 100 200 300 400 Time (min) Fig. 1. The concentration of the tears from the left (D) and right eyes of a salt- gland-cannulated turtle during the salt gland response. Injection solutions of 3mol 1 \l-5moll * and 0-75 moll l NaCl were made by dissolving the appropriate amount of NaCl in deionized, distilled water and then filtering this mix through a 0-45 /«n filter. Next, the solution was autoclaved and finally transferred to sterile bottles in a clean room.
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